Synopsis of the ticks of Algeria with new hosts and localities records

Background Ticks are obligate hematophagous arthropods with a world-wide distribution that are extremely important not only in terms of human and animal health but also economically. In Algeria, information on tick species is scarce. Methods A systematic literature review was performed using online databases. The information extracted from the databases was was supplemented by information from an original study. Ticks were collected from various hosts and by flagging from January 2018 to December 2019. Results To date, in Algeria a total of 36 valid tick species belonging to two families have been recorded: (1) family Argasidae, with three Argas species and nine Ornithodoros species recorded; and (ii) family Ixodidae, with one Dermacentor species, three Haemaphysalis species, 10 Hyalomma species, four Ixodes species and six Rhipicephalus species recorded. The geographical distribution for each species was determined and listed. Eight new tick-host associations were recorded: four for Ixodes inopinatus sensu Estrada-Peña et al. 2014, one for Rhipicephalus bursa, one for R. turanicus, one for Hyalomma marginatum and one for Hy. lusitanicum. To our best knowledge, this study is the first to report the presence of I. inopinatus sensu Estrada-Peña et al. 2014 in Algeria. We also report here for the first time all tick species (Argasidae and Ixodidae) known to be present in Algeria. Conclusion This article represents a tool for students and scientists who work in the field of ticks and provides important new data on the distribution of ticks in Algeria. Graphical Abstract Supplementary Information The online version contains supplementary material available at 10.1186/s13071-022-05424-2.


Background
Ticks are hematophagous arthropods that represent major potential hazards to human and animal health [1,2]. There are over 900 tick species worldwide, divided into three families: the Ixodidae (hard ticks), Argasidae (soft ticks) and Nutalliellidae [3]. Ticks feed on various vertebrate hosts, passing through three active developmental stages (larva, nymph, adult). Depending on the behavior of each species, they may parasitize one, two or three hosts during a life-cycle. Ticks have a worldwide geographic distribution that is conditioned by biotic (temperature and humidity) and abiotic (host) factors. As a result, ticks are predisposed to harboring several types of microorganisms, including bacteria, viruses and parasites, and are therefore closely associated with the emergence of vector-borne diseases. Ticks play an important role in human and animal health as potential transmitters of a range of pathogens and can be the cause of significant economic losses. Therefore, ticks represent an important subject of research.
A total of 91 tick species have been reported in the Palearctic region, of which 67 species have been recorded in Europe and North Africa [4,5]. Algeria is the largest country in Africa, the largest country in the Mediterranean Basin, and the tenth largest country in the world, with a surface area equivalent to 56% of the European Union's (EU) total land area. Surprisingly, despite its vastness, habitat and climate diversity, little data are currently available on the diversity and distribution of tick fauna in this country. The first published research on ticks dates back to the first half of the twentieth century when Senevet [6] and Senevet and Rossi [7] studied the distribution of cattle ticks and the cattle tick-host association. More recently, several studies have been conducted on ticks and tick-borne diseases in Algeria [8][9][10][11][12][13], but significant knowledge gaps remain. We have therefore perfomed a systematic literature review and used the extracted data to update the knowledge on the diversity, geographical distribution and host association of tick species present in Algeria. We also highlight curent knowledge gaps to promote more targeted research.

Systematic literature review
The systematic literature review was performed according to the PRISMA 2020 protocol [14]. The search queries were done in online databases (PubMed, Google Scholar and Science Direct). Key terms searched in the title, abstract and/or keywords of studies were: "ticks AND Algeria, " "tiques AND Algérie, " "Ixodidae AND Algeria, " "Ixodidae AND Algérie, " "Argasidae AND Algeria" and "Argasidae AND Algérie", which allowed the inclusion of both English and French literature. To ensure that all publications were included in the search, we also performed reverse reference tracking. Inclusion criteria were: (i) study area was within the territory of Algeria; and (ii) the data included the exact or approximate location of tick collection. No exclusion criteria were applied. From each paper, the following data were extracted (if available): tick species, stage, host species, sample size, prevalence, location with georeferenced information (decimal degree coordinate), the precision of the location (on a scale of 1-4, with 1 indicating that exact coordinates were known, 2 indicating that locality was known; 3 indicating that region/county was known; 4 indicating that location was unknown) and bibliographic source. The reported binomial names of tick species were updated to those currently accepted, according to the most recent taxonomical opinions [4].
All data were entered into a tabular database system (Microsoft Excel; Microsoft Corp., Redmond, WA, USA). All raw data are provided in Additional file 1: Table S1. The digital maps were made using QGIS version 3.14.

Original data
In addition to using data extracted from the literature, we collected ticks from various animal hosts and by flagging in several localities of Algeria from January 2018 to December 2019. These data are also available in Additional file 1: Table S1. All collected ticks were preserved in 70% ethanol. The collected specimens were separated by developmental stage and sex and identified to species level using morphological characteristics according to Estrada-Peña et al. [15].

Results
Overall, the database resulting from this study includes 171,929 individual ticks, in 36 species (12 Argasidae and 24 Ixodidae) in a total of 853 records. The distribution maps for each tick species are shown in Figs. 1-9, respectively, and discussed in detail in the Discussion. The overview of tick-host associations and the synoptic list of ticks are shown in Tables 1 and 2.

Literature data
Overall, data were extracted from 56 papers (Additional file 1:

Discussion
The tick fauna of Algeria has been reported in several historical studies as well as in more recent papers. However, there have been no studies on the ticks of southern Algeria, and only 26 records (3.05%) of all reported records are from latitudes below 30°N. Most records (n = 617; 72.33%) are from the northern part of the country (between 35°N and 36°N) (Fig. 1). This suggests a huge gap in knowledge on tick diversity and distribution across most of Algeria's territory. Our study reports eight new tick-host associations for Algeria. We also report for

Genus Argas
Three Argas species have been reported in Algeria. Argas persicus was reported only on a few occasions and only from domestic poultry. Most records are from the north of the country, with only one record from the south (Fig. 2). This is consistent with the ecology of the species, which is known to be an endophilic tick present in the desert, temperate Mediterranean regions and rainforests [16].
The two other Argas species recorded in Algeria are both bat specialists. Argas transgariepinus was reported from two vespertilionid bats in the northern part of the country (Fig. 2). Argas vespertilionis is an endophilic tick that was reported in Algeria in bats of belonging to the genera Plecotus and Tadarida, respectively ( Fig. 2)

Genus Ornithodoros
Nine species belonging to this genus have been found in Algeria, most of them parasitic on wild birds. Ornithodoros capensis is a nesting tick species that specializes on seabirds [17], with a worldwide distribution in the Pacific, Atlantic and Indian Oceans and in East Africa's Rift Valley. In Algeria, O. capensis has been found infesting nests of the seabird Larus michahellis (Fig. 3).
The range of O. savignyi in Africa is relatively wide, extending across most of the continent's regions [16]. In Algeria, this tick was found on camels (Fig. 3) (Fig. 3).

Genus Dermacentor
Dermacentor marginatus is the only species of this genus recorded in Algeria. Adult ticks feed on sheep, cattle, goats and dogs, and larvae and nymphs parasitize small mammals, mainly rabbits, and birds [16]. In North Africa, D. marginatus shares the same habitat as Ixodes ricinus [16]. In Algeria, D. marginatus ticks were reported on two mammal species distributed in the country's northern region, mainly at high altitudes ( Fig. 4), suggesting a co-distribution relationship with wild boar.

Genus Haemaphysalis
Three species of genus Haemaphysalis were reported from Algeria, with most reports mentioning Ha. sulcata and Ha. punctata; there is only a single report of Ha. erinacei, collected from the desert hedgehog Paraechinus aethiopicus and the North African hedgehog Atelerix algirus, occurring in the northern part of the country, in a steppe area (Fig. 5).
Haemaphysalis punctata is a three-host tick which parasitizes cattle and sheep and occasionally also horses, goats and antelopes. This tick is distributed throughout Europe, North Africa and East Asia [16]. In Algeria, it was found on cattle, but infestations on sheep, wild boars and dogs have been reported. It is present in the northern part of the country (Fig. 5).
Haemaphysalis sulcata is also a three-host tick, with sheep being the most common host. This tick occurs over a wide range in North Africa, Europe and Asia [19][20][21]. In Algeria, it is found on sheep, cattle and goats and is localized in the country's northeastern part (Fig. 5).

Genus Hyalomma
This genus is the most diversified in terms of the number of species reported from Algeria and 10 species of genus Hyalomma have been reported in Algeria. Hyalomma aegyptium is a three-host tick with tortoises of genus Testudo being the main hosts for all developmental stages. This tick is present in the Mediterranean basin and in the Black Sea [22]. In Algeria, Testudo greaca is the main and only reported host for Hy. aegyptium. This tick has been reported in the northern and interior regions of the country, as its distribution is dependent on the presence of its host, as shown in previous studies [23] (Fig. 6).
Hyalomma anatolicum is an endophilic tick with a two-or three-host life-cycle. Large ungulates, mainly cattle, horses, camels, sheep and goats are hosts for all developmental stages [24]. This tick is widely distributed throughout Africa and Asia [21]. In Algeria, Hy. anatolicum is reported on livestock and is present in the northern, interior and southern regions of the country (Fig. 6).
Hyalomma dromedarii has a two-or three-host lifecycle. The camel is the preferred host, but domestic mammals can also harbor this tick. Hyaloma dromedarii occurs in Mediterranean, steppe and desert climates [16]. It is reported mainly on camels in Algeria, but    n/a [38] Felis catus A [12] and current study infestations on sheep have been reported in Algeria [25]. The presence of Hy. dromedarii is strictly associated with the geographical distribution of its main host, the dromedary (Fig. 6).
Hyalomma excavatum is a two-or three-host exophilic tick, with domestic mammals being frequent hosts but cattle and camels being the main ones. Insectivores, lagomorphs and rodents are the preferred hosts of the immature stages. This tick species is known to occur in North Africa, East Africa, southern Europe, the Middle East and Central Asia [21,24]. In Algeria, it is reported from livestock (Fig. 6).
Hyalomma impeltatum has a two-or three-host lifecycle. Members of family Camelidae and family Bovidae are the common hosts for adults, while those of Leporidae (rabbits and hares) and Muridae (small rodents) are common hosts for immature stages [4]. Hyalomma impeltatum is widespread in the Palearctic region [26]. In Algeria, it is reported on livestock, with the dromedary as the most common host (Fig. 6).
Hyalomma lusitanicum is a three-host tick feeding on cattle and other domestic and wild ungulates. It is restricted to the western part of the Mediterranean subregion of the Palearctic zoogeographical region [27]. In Algeria, it has been collected from five mammalian hosts (Fig. 6).
Hyalomma marginatum is a two-host tick with mammals as the primary hosts. Its geographical distribution includes southern Europe and North Africa [28]. In Algeria, Hy. marginatum is the most reported species of its genus (Fig. 7).
Hyalomma rufipes is a two-host exophilic tick. Adults feed on cattle, sheep, goats, horses and camels. Larvae and nymphs infest birds and leporids [27]. In Algeria, it seems to have a broad range (Fig. 7).
Adult and immature stages of Hy. scupense feed primarily on cattle and horses but there may have been rare sightings on sheep, donkeys, pigs, camels and wild Hypsugo savii n/a [86] Hepestes ichneumon A [11] Miniopterus schreibersii n/a [86] Myotis cappaccinii n/a [86] Myotis punicus n/a [86] Ovis aries n/a [25]     ungulates [29]. Hyalomma scupense has a broad distribution, ranging from North Africa and Western Europe to the eastern parts of China [30]. In Algeria, cattle are reported as the preferred host of Hy. scupense, but infestations on other domestic ungulates have also been reported (Fig. 7). Domestic herbivores are the preferred hosts of the adult of Hy. truncatum, while immature stages parasitize hares and rodents [16]. This tick species has been reported in the northern and southern parts of Algeria infesting cattle and camels (Fig. 7).

Genus Ixodes
Four species of the genus Ixodes were reported in Algeria. Ixodes hexagonus is a three-host species with carnivorous mammals and hedgehogs as the main hosts. It has a wide distribution in Europe [31], but in Algeria only two reports are available on this tick, collected from dogs and hedgehogs (Fig. 8).
Ixodes inopinatus sensu Estrada-Peña et al. 2014 is an exophilic tick. The immature stages feed on lizards and adults feed on red foxes and sheep [32,33]. Earlier studies reported its presence in Spain, Portugal, Tunisia and Morocco [32], but more recently it has also been reported in Eastern Europe and Tunisia, in sympatry with I. ricinus [33,34]. In Algeria, prior to our report, no data were available regarding I. inopinatus sensu Estrada-Peña et al. 2014 [32], as previously any specimens may have been misidentified as I. ricinus. In the current study, immature stages were collected from lizards while adults  were collected from cattle, providing new host association records for the country. It is important to note that we collected this species in a forest habitat (Quercus spp.). Its distribution range in Algeria is the northeastern region (Fig. 8). However, given the lack of surveys, we assume it is more widespread than we expect and may be spread at least over the northern region of the country.
Ixodes ricinus is a three-host tick with catholic behavior. Immature stages parasitize birds and lizards, while mammals are the preferred hosts for adults [15]. This tick is present in the Western Palearctic region in terms of its range, with over 300 host species. In Algeria, the reported hosts include nine mammals and three reptile species. The adult stage has been found on mammals and the immature mainly on lizards. Its distribution is limited to the northern part of Algeria, mainly in the mountainous regions (Fig. 8).
Ixodes vespertilionis is a three-host, endophilic tick that parasitizes bats and is widely distributed in Europe [35]. In northern Algeria, previous reports have reported infestation by tick of troglodyte bats [36] (Fig. 8).

Genus Rhipicephalus
The genus Rhipicephalus is represented in Algeria by six species, all of which are fairly abundant in most of the domestic hosts. This tick feeds on the same host during all developmental stages, with the preferred hosts being ruminants, but infestations of wild boar and cats are also frequently reported [16]. In Algeria, R. annulatus is mainly located in the country's northern region which is characterized by a dominant Mediterranean climate. Previous studies have shown that cattle are the main host in Algeria, but infestations on other mammals (dogs, horses, goats and sheep) have also been reported [12,[37][38][39] (Fig. 9).
Rhipicephalus bursa is a two-host tick that feeds on various mammals. The geographical distribution of R. bursa extends around the Mediterranean Sea [40]. In Algeria, it has been collected from cattle, sheep, goats, horses, dogs, cats and hedgehogs [11,12,41,42]. This report reveals its presence on wild boars for the first time, constituting a new host association for Algeria. Its distribution is limited to the northern region of the country (Fig. 9).
Rhipicephalus evertsi evertsi is a two-host tick that feeds on cattle and wild ungulates and has a teletropic feeding behavior. This tick is widespread throughout African countries, with a preference for the Afrotropical zoogeographic region [40]. In Algeria, R. evertsi evertsi was reported sporadically on sheep and camels in the southern part of the country by Bouhous et al. [25,43]; however, these authors suggested that it could be an accidental infestation (Fig. 9).
Rhipicephalus guilhoni has a three-host life-cycle, with adult ticks infesting mammals (horses, cattle, sheep, dogs and wild carnivores) and immature stages feeding on small mammals. This tick has a range in Africa that extends from Senegal to Ethiopia [40]. Only one report is known for Algeria, with ticks collected on sheep, located in the south of the country [25] (Fig. 9).
Rhipicephalus sanguineus sensu lato (brown dog tick) is the most widespread tick in terms of its host spectrum in Algeria, which includes 15 mammalian species [8,11,12,[44][45][46]. It is a three-host tick that feeds mainly on dogs but can be found on other hosts [47]. In Algeria, R. sanguineus s.l. has been found in domestic fauna (dogs, camels, goats, cattle, cats and sheep) and wildlife (jackal, bats, hedgehog, wild boar and mongoose). In this study, we report it in cattle, dogs, sheep, cats and hedgehogs. Only the adult stage was reported from the hosts, while the immatures were collected by flagging [48]. The brown dog tick has a worldwide distribution. In Algeria, it is present in the northern, central and southwestern regions of the country (Fig. 9).
Rhipicephalus turanicus is present in the Palearctic region, although its actual distributional boundaries remain unclear due to its ambiguous phylogeny [4]. This species is a three-host tick. In Algeria, it is present in the northern part of the country where it infests cattle, goats, dogs, wild boars and hedgehogs [8,37,42,49,50] Interestingly, we collected it from cats, which is a new host association for Algeria (Fig. 9).
To summarize, due to the global changes that have taken place in recent years, Algeria is facing desertification [51]. The absence of ecological barriers between Algeria and neighboring countries, the legal and illegal movement of animals in the North African region and the different types of livestock farming practiced in Algeria (e.g. nomadism, pastoralism, and transhumance) are factors potentially responsible for a high diversity and geographical distribution of ticks. However, from the data presented in this article, it is clear that there are several gaps in data regarding tick diversity and distribution in Algeria. Despite the high wild terrestrial vertebrate diversity in this country (111 mammals, 406 birds and 99 reptiles) [52][53][54], there are surprisingly few studies on their ticks. Moreover, vast territories of the country remain completely unstudied for ticks. Future approaches to fill these gaps can reveal the presence of so far unreported tick species for Algeria.

Conclusions
This study is the first to report the presence of Ixodes inopinatus sensu Estrada-Peña et al. 2014 in Algeria and provides valuable and important new important data on the distribution of ticks and new tick-host associations.
Additional file 1: Table S1. Data analyzed in the current study.